Role of olfaction and vision in homing behaviour of black rockfish Sebastes inermis

Journal of Experimental Marine Biology and Ecology 322 (2005) 123 – 134 www.elsevier.com/locate/jembe

Role of olfaction and vision in homing behaviour of black rockfish Sebastes inermis Hiromichi Mitamuraa,T, Nobuaki Araia, Wataru Sakamotob, Yasushi Mitsunagac, Hideji Tanakad, Yukinori Mukaie, Kenji Nakamurae, Masato Sasakif, Yoshihiro Yonedaf a

Graduate School of Informatics, Kyoto University, 606-8501, Japan b Fisheries Laboratory of Kinki University, 649-2211, Japan c Faculty of Agriculture, Kinki University, 631-8505, Japan d COE for Neo-Science of Natural History, Graduate School of Fisheries Science, Hokkaido University, 041-8611, Japan e Chateau Marine Survey Co., Ltd., 534-0025, Japan f Kansai International Airport Co., Ltd., 549-8501, Japan Received 11 November 2004; received in revised form 14 February 2005; accepted 15 February 2005

Abstract How fish find their original habitat and natal home remains an unsolved riddle of animal behaviour. Despite extensive efforts to study the homing behaviour of diadromous fish, relatively little attention has been paid to that of non-diadromous marine fish. Among these, most rockfish of the genus Sebastes exhibit homing ability and/or a strong fidelity to their habitats. However, how these rockfish detect the homeward direction has not been clarified. The goal of the present research was to investigate the sensory mechanisms involved in the homing behaviour of the black rockfish Sebastes inermis, using acoustic telemetry. Vision-blocked or olfactory-ablated rockfish were released in natural waters and their homing behaviours compared with those of intact or control individuals. Blind rockfish showed homing from both inside and outside their habitat. The time taken by blind fish to reach their home habitat was not significantly different from that of the control fish. In contrast, most olfactory-ablated fish did not successfully reach their original habitat. Our results indicate that black rockfish predominantly use the olfactory sense in their homing behaviour. D 2005 Elsevier B.V. All rights reserved. Keywords: Biotelemetry; Black rockfish; Homing; Olfaction; Vision

1. Introduction T Corresponding author. Tel: +81 75 753 3137; fax: +81 75 753 3133. E-mail address: [email protected] (H. Mitamura). 0022-0981/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2005.02.010

Some marine fish have homing ability and a strong fidelity to their habitats and spawning sites. Salmonids return to their natal rivers to spawn (Hasler and Scholz, 1983; Dittman and Quinn, 1996). The olfactory system

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of salmon is necessary for home-stream detection, and salmon are also very sensitive to the odours that emanate from conspecific fish (Doving and Stabell, 2003). Among demersal fish, the homing of the Atlantic cod to its spawning grounds is well known (Green and Wroblewski, 2000; Rawson and Rose, 2000; Robichaud and Rose, 2001). Individual cod range widely but each year return over some hundreds of kilometres to their specific spawning grounds. Plaice also migrate between feeding and spawning grounds, and selective tidal-stream transport is a key factor in their migratory mechanism (Metcalfe et al., 1990, 1993; Arnold and Metcalfe, 1996). Attempts to explain homing orientation have evoked a great variety of proposals regarding the sensory mechanisms involved. However, the long-distance migrations of fish make it difficult to observe homing behaviours in the sea. It has been recognized since the 1970s that many rockfish of the genus Sebastes also exhibit homing ability and a strong fidelity to their habitats if displaced (Carlson and Haight, 1972; Larson, 1980; Love, 1980; Matthews, 1990; Pearcy, 1992; Starr et al., 2000, 2002; Love et al., 2002). For example, the black rockfish Sebastes inermis exhibits fidelity to its habitat (Numachi, 1971; Shinomiya and Ezaki, 1991) and can return to its origin after displacement of 1–4 km for some days (Mitamura et al., 2002). The genus Sebastes includes about 100 species (Jordan et al., 1930; Kendall, 1991; Love et al., 2002), and all of them may display homing ability and strong fidelity to their habitats (Matthews, 1990; Love et al., 2002). Moreover, the sensory mechanisms they use in returning to their habitats seem to be common to rockfish of the genus Sebastes (Matthews, 1990). However, while previous research focused on the homing patterns, activity patterns, and habitat preferences of these fish, no studies have been undertaken to determine how the rockfish finds its habitat (Love et al., 2002). The black rockfish grows relatively slowly, is longlived (Harada, 1962; Hatanaka and Iizuka, 1962; Yokogawa and Iguchi, 1992; Utagawa and Taniuchi, 1999) and is a typical site-specific fish. Generally, compared with mobile pelagic fish, site-specific fish are more likely to learn landmarks because they inhabit areas with distinctive features, such as are found in rocky habitats (Dodson, 1988; Reese, 1989). This suggests that the rockfish, including the black rockfish, may use visual cues such as landmarks or

topographic features when homing (Matthews, 1990; Mitamura et al., 2002; Love et al., 2002). Some reports have suggested that the olfactory sense is also used as a navigational cue in rockfish homing (Matthews, 1990; Mitamura et al., 2002). Many rockfish have a relatively small home range (Love et al., 2002). However, long-distance homing from as far away as 22.5 km has been reported (Carlson and Haight, 1972), suggesting that rockfish home from outside their habitats. In other displacement experiments, rockfish initiated their homing journey with small random movements around the release site, and then moved into a fixed direction towards their home (Matthews, 1990; Mitamura et al., 2002). This fact also suggests that rockfish can start the homeward journey from outside their home range in which familiar visual landmarks would occur. The objective of this study was to detect the primal cue for homing in displaced black rockfish. We focused on visual cues and olfactory cues, and conducted experiments with both vision-blocked and olfactory-ablated fish.

2. Methods 2.1. Tagging with coded ultrasonic transmitters All fish (Table 1) used in the visual-cue and olfactory-cue experiments were over 150 mm in total length and were considered to be mature (Mio, 1960; Yokogawa et al., 1992). We used ultrasonic coded transmitters (V8SC-6L; Vemco Ltd., Nova Scotia, Canada) that are 8.5 mm in diameter, 25 mm long, and weigh 2.2 g in water. The transmitter was implanted surgically into the peritoneal cavity of the fish in accordance with the Japan Ethological Society guidelines for the experimental use of animals. Surgical treatments were carried out under anaesthesia induced with 0.1% 2-phenoxyethanol. The implant operation took approximately 5 min. The fish was placed between rubber sponges in a bath of fresh bubbling seawater throughout the operation. An incision about 10 mm in length was made in the abdomen of the fish and the transmitter was inserted. The wound was closed with an operating needle and sutures. The antibiotics oxytetracycline hydrochloride and polymixin B sulfate were applied. The fish were held in a

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Table 1 Summary of treatment, total length, date monitoring began, date monitoring finished, homing duration, and time of day when homing, type of homing performance, capture point, release point, and site of final destination of the tagged fish ID

Treatment

Total length (mm)

Date monitoring began

Date monitoring finished

Homing duration (days) and time of day when homing

Type of homing performance

Captured point

Release point

Site of final destination

B01 B02 B03 T01 T02 T03 B04 B05 B06 B07 T04 T05 T06 T07 I01 I02 I03 I04 OA01 OA02 OA03 OA04 OA05 OA06

Black Black Black Transparent Transparent Transparent Black Black Black Black Transparent Transparent Transparent Transparent Intact Intact Intact Intact Olfactory ablation Olfactory ablation Olfactory ablation Olfactory ablation Olfactory ablation Olfactory ablation

230 230 215 220 190 220 247 215 202 255 220 250 230 235 240 225 215 240 245 180 210 240 215 225

05-Apr-01 05-Apr-01 05-Apr-01 05-Apr-01 05-Apr-01 05-Apr-01 14-May-01 14-May-01 14-May-01 14-May-01 14-May-01 14-May-01 14-May-01 14-May-01 16-Nov-01 16-Nov-01 16-Nov-01 16-Nov-01 16-Nov-01 16-Nov-01 16-Nov-01 16-Nov-01 16-Nov-01 16-Nov-01

09-Apr-01 09-Apr-01 09-Apr-01 09-Apr-01 09-Apr-01 09-Apr-01 22-May-01 22-May-01 22-May-01 22-May-01 22-May-01 22-May-01 22-May-01 22-May-01 28-Nov-01 28-Nov-01 28-Nov-01 28-Nov-01 28-Nov-01 28-Nov-01 28-Nov-01 28-Nov-01 28-Nov-01 28-Nov-01

1, 1, 1, 1, N 2, 1, 1, N 1, 1, 1, 1, 1, 1, 7, 1, 3, N 5, N N 5, N

3a 3a 3a 3a N 3a 3b 3b N 3b 3b 3b 3b 3b 4a 4a 4a 4a 4b 4d 4c 4c 4d 4c

X X X X X X X X X X X X X X B B A A B A A B A B

Y Y Y Y Y Y Z Z Z Z Z Z Z Z A A B B A B B A B A

X X X X Other X X X Other X X X X X B B A A Other A Oil-tanker berth Oil-tanker berth A Oil-tanker berth

Dusk Dusk Dusk Dusk Dawn Daytime Daytime Daytime Daytime Midnight Midnight Dusk Midnight Midnight Dawn Midnight Midnight

Midnight

The dashed line on the table separates the visual-cue and olfactory-cue experiments. The identity designations B02 and T06, B03 and B05, and T01 and T04 specify the same fish. N means no homing. bTime of day when homingQ means the time during the day when the fish homed: daytime, 9:00–17:00; dusk, 17:00–21:00; midnight, 21:00–5:00; dawn, 5:00–9:00. bType of homing performanceQ means the typical homing path described in Figs. 3 and 4. X, Y, Z, A, B, and oil-tanker berth are the sites shown in Figs. 1 and 2. Other means other sites. bSite of final destinationQ means the place the fish was located at the end of the experiment.

circular plastic experimental tank (1 m3 in volume) for about two days to allow them to recover from surgery. Sufficient fresh bubbling seawater was exchanged. No effects of surgery on the behaviour of the fish were observed. Preliminary experiments using dummy transmitters demonstrated that intraperitoneal implantation had no discernible effects on feeding or swimming behaviour over a period of about a month. 2.2. Tracking and monitoring systems Three types of systems (five VR1, 10 VR2, and one VR28 systems [Vemco Ltd.]) were used to track and monitor tagged fish. The tracking system on the research vessel (VR28 system) had four hydrophones that detected fish direction. Signals from the coded

transmitters were received through a four-channel receiver by the hydrophone system, and the receiver was connected to a personal computer. The relative receiving strengths from the four hydrophones were used to determine the direction of an individual fish. The ID number of the coded transmitter and the position of the vessel established from GPS (Garmin Ltd., Olathe, KS, USA) were recorded. Garmin GPS receivers are accurate to within 15 m on average. The position of a fish was recorded when the receivers detected signals from that fish (when the tagged fish was within about 20 m of the receivers). The monitoring system for the fixed receivers (VR1 and VR2 systems) was 60 mm in diameter and 340 mm long and logged data on the presence of fish tagged with a coded transmitter. The system had a

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flash memory to record data and was powered by a lithium battery that lasts for up to 180 days. The receiver was installed at mid-water depth between the release point and their original habitat. The ID number, date, and time were recorded when a tagged fish passed within 300–500 m of the receiver. We installed five fixed monitoring receivers in Maizuru Bay in the visual-blocked experiments, and 10 fixed monitoring receivers around the Kansai International Airport (KIX) island in the olfactory-ablation experiment. In both experiments, the areas between the release points and the capture sites were monitored by these monitoring systems (Figs. 1 and 2).

2.3. Visual-cue experiments The experiments on visual cues were conducted at Maizuru Bay (Fig. 1). It is about 5–20 m deep, and the coastline is complex and often rocky. Eleven black rockfish were collected by angling or in fish traps within a radius of about 10 m of point X (Fig. 1). Whereas two fish (ID B01 and T03) were captured about five months before release, the remaining nine fish were captured just before their release due to the difficulty in collecting more than several black rockfish at one time in this study site. All fish sampled were kept in tanks before experimental

Fig. 1. The study site, fish capture and release sites, and receiver locations in the visual-cue experiments in Maizuru Bay. (a) Study site of visualcue experiment 1; (b) study site of visual-cue experiment 2. Dashed circles represent the expected signal detection ranges of the coded ultrasonic transmitters.

H. Mitamura et al. / J. Exp. Mar. Biol. Ecol. 322 (2005) 123–134

N

127

Vertical seawall Gently sloping seawall

1

KIX

A 2

10

3 4 Tidal current direction

5 6

Tanker berth

7 8

B

Capture and release point

9 1 km Nursery area

Fig. 2. The study site, fish capture and release points, and receiver location of the olfactory-cue experiment in Osaka Bay. Ten automated receiver systems were set up to cover the entire seawall of Kansai International Airport. Dashed circles represent the expected signal detection ranges of the coded ultrasonic transmitters.

release. To eliminate vision, we attached a mask of black polyvinyl chloride over the eyes using the method of Lohmann et al. (1995) and Larisa and Lohmann (2003). This eliminated any impact on the fish’s breathing. Transparent polyvinyl chloride was used on the control fish. Preliminary laboratory experiments indicated that the mask lasted for approximately one week. Two fish that had been kept for 5 months were divided among the blind and the control fish to remove the bias of data from their long-term captivity. In the first release experiment, three vision-blocked fish and three with transparent masks, were released on 5 April 2001 at point Y, about 1000 m east of the capture point and in water about 12 m deep (Fig. 1). Four fish (B02, B03, T01, and T03) were recaptured within 20 days in fish traps installed at the capture site. In the second experiment, four vision-blocked fish and four with transparent masks, including fish B02, B03, and T01 recaptured in the first experiment

(Table 1), were released on 14 May 2001 at point Z, about 150 m west of the capture point and in water about 7 m deep (Fig. 1). Using a research vessel, we tracked the fish continuously for about 8 h immediately after release and for about 3 h on the following day. Tracking was conducted primarily around the capture and release points. We also monitored tagged fish using five monitoring receivers over five and nine days after release around the capture and release points, respectively. 2.4. Olfactory-cue experiment In Maizuru Bay, three individual fish were used in multiple experiments because it was difficult to collect several fish in a short period. Therefore, we moved the study site for the subsequent experiment to KIX (Fig. 2). Commercial fishing has been prohibited in the KIX island area, where black rockfish are sufficiently abundant for our study. The sea around the KIX island

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is 18 m deep and the sea floor is extremely soft. Most of the seawall (8.7 km) around the KIX island is in the form of a gently sloping rubble mound. The mound is covered by many kinds of seaweed and is used as a spawning and nursery area for marine animals. Ten black rockfish were collected within a radius of about 100 m from points A and B near the eastern seawall of the KIX island (Fig. 2). All fish sampled were kept for about four or five days in tanks before experimental release. To eliminate olfaction, we plugged the olfactory pits of the rockfish with petroleum jelly, using the method of Wisby and Hasler (1954), Hasler and Scholz (1983), and Yano and Nakamura (1992). We kept 10 black rockfish with petroleum jelly in their nares in a tank to determine how long the petroleum jelly remained in place. All control and olfactory-ablated fish were released approximately 2 km from the capture point on 16 November 2001. We monitored the tagged fish for 13 days after release using the 10 fixed monitoring receivers. 2.5. Statistical analysis The times taken to reach home were compared between the fish with black masks and those with transparent masks in the visual-cue experiments using a t-test after data standardization using square-root transformation (Zar, 1996). The Mann–Whitney Utest was used to compare the homing times of intact and olfactory-ablated fish in the olfactory-cue experiment. In order to compare these homing times, the reciprocals of the times were used. The Kruskal– Wallis test was used to compare the total body lengths and weights of fish between groups at the two capture points and the oil-tanker berth (Fig. 2).

3. Results

In vision-blocked experiment 1, all blind fish and two of three control fish returned to the capture site between dusk and dawn within two days (Table 1). The time taken for the blind fish to home was not significantly different from that of the control fish (ttest: N blind = 3, mean: 0.71 min 1, upper and lower limit confidence: 0.71 min 1, N control = 3, mean: 0.71 min 1, upper and lower limit confidence: 0.71 min 1, P N 0.05). The homing paths taken by the blind fish were almost the same as the paths taken by the control fish (Fig. 3a). Once the tagged fish had returned to their original site, they were not tracked or monitored around the release point until the end of the experiment (Fig. 3a). The control fish (T02) that failed to home moved in a direction away from the capture site, and could not be tracked or monitored to determine its ultimate fate. This fish was the smallest in the experiment. Fish B01 and T03, which had been kept in a tank for about five months before release, returned to the capture site. In vision-blocked experiment 2, three of the four blind fish and all the control fish returned to the capture site within one day (Table 1). The time taken by the blind fish to home was not significantly different from that taken by the control fish (t-test: N blind = 4, mean: 0.71 min 1, upper and lower limit confidence: 0.70 and 0.72 min 1 N control = 4, mean: 0.71 min 1, upper and lower limit confidence: 0.70 and 0.72 min 1, P N 0.05). The homing paths taken by the blind fish were almost the same as the paths taken by the control fish (Fig. 3b). In contrast to visionblocked experiment 1, the tagged fish that homed were tracked and monitored near the release point after homing (Fig. 3b). The blind fish (B06) that failed to home returned to the capture site at dusk and subsequently moved from the capture site to the point designated point A in Fig. 1. It did not return to the capture site. This fish was the smallest fish in the experiment. Fish B07, which had been kept in a tank for about five months before release, returned to the capture site.

3.1. Visual-cue experiments 3.2. Olfactory-cue experiment In both visual-cue experiments, six of the seven blind fish and six of the seven control fish returned to the capture site. Among the 12 fish that homed, eight returned to the capture site under low light conditions between dusk and dawn (Table 1).

The laboratory experiment showed that the petroleum jelly remained in their nares for 5–10 days. Plugging with petroleum jelly had no significant effect on feeding or swimming behaviour.

Original site

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a) Exp. 1 5 4 Control fish

2 1 5-Apr.

7-Apr.

4 Blind fish

3 2 1 5-Apr.

7-Apr.

Release site

4

9-Apr.

b) Exp. 2

3

Original site

2

Control fish

1 14-May 16-May 18-May 20-May 22-May 24-May 4 Receiver location

Release site Original site

9-Apr.

5 Receiver location

Release site

Original site

Release site

3

3

2

Blind fish

1 14-May 16-May 18-May 20-May 22-May 24-May

Fig. 3. Typical homing paths of tagged black rockfish in the visual-cue experiments. (a) Shows the results of visual-cue experiment 1 and (b) those of visual-cue experiment 2. The dashed line on the graph separates visual-cue experiments 1 and 2.

All control fish returned to their capture sites almost directly under low light conditions between dusk and midnight within seven days (Table 1, Fig.

4a). Four of the six experimental fish did not return to the capture site. One of them moved in the opposite direction to the capture site and could not

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3 2 1 10 16-Nov.

Release site

19-Nov.

22-Nov.

25-Nov.

28-Nov.

9 8 7 6 5 4 3 2 1 10 16-Nov.

b) Olfactory Ablation fish. No homing.

19-Nov.

22-Nov.

25-Nov.

28-Nov.

9 8

Release site

7 6 5 4 3 2 1 10 16-Nov.

c) Olfactory ablation fish. Staying at another site.

19-Nov.

22-Nov.

25-Nov.

28-Nov.

9 8 Receiver location

Original site Release site Original site

a) Intact fish Directly homing.

4

Original site

Original site

Release site

9 8 7 6 5

7 6 5 4

d) Olfactory ablation fish Straying and then homing after loss of ablation jelly.

3

2 1 10 16-Nov.

19-Nov.

22-Nov.

25-Nov.

28-Nov.

Fig. 4. (a) Shows the typical homing path of an intact fish in the olfactory-ablation experiment. (b–d) Show the typical movements of three experimental fish with olfactory ablation.

be tracked or monitored (Fig. 4b). The other three moved back and forth along the seawall and ultimately stayed in the area of stations 5 and 6

(Fig. 4c). Stations 5 and 6 were located around an oil-tanker berth built on many piles. The piles provide numerous species with a feeding ground

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and living space. The black rockfish around the oiltanker berth (Mitamura et al., 2002) were significantly larger in body size and weight than those found around points A and B (Kruskal–Wallis test: H = 7.050, df = 2, P b 0.05) (Fig. 2). These three experimental fish remained in this high-quality habitat. The other two experimental fish homed. They stayed mainly around the oil-tanker berth after release (Fig. 4d). They then moved back and forth between the capture and release points along the seawall and finally homed at midnight five days after release (Fig. 4d). Because the petroleum jelly would have remained in their nares for 5–10 days, they appeared to home after the time at which the petroleum jelly would be lost from their nares. Therefore, the time taken by the experimental fish to home was significantly longer than that taken by the intact fish (Mann–Whitney U-test: N intact = 4, N olfactory ablation = 6, P b 0.05).

4. Discussion 4.1. Homing mechanism Our results indicate that the black rockfish primarily uses olfaction to return to its home habitat, and does not appear to use visual cues for homing. In both vision-blocked experiments, the homing durations of the control fish were slightly longer than those of the blind fish although there was statistically no difference between them (Table 1). This reinforces the results that the rockfish does not appear to use visual cue for homing although the low sample size might mask the effect of vision-blocked treatment. Researchers have thought that rockfish, including the black rockfish, use visual cues for homing because displaced rockfish were found on or near reefs and rocky areas on their return routes (Matthews, 1990; Love et al., 2002; Mitamura et al., 2002). The use of landmarks for homing requires a familiar landmark around the release site, one which the animals have previously used to move to their destination (Fred, 1998). In vision-blocked experiment 2, the tagged fish were tracked and monitored after they returned to their original site around the release point until the end of the experiment (Fig. 3b). These results imply that the release points in

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this experiment were inside the home range of these fish. However, our results show that the time taken and the homing paths did not differ between the blind fish and control fish. This suggests that the black rockfish might not use vision for homing inside its home range. Homing from outside the familiar site was also examined. In both the olfactory-ablation experiment and vision-blocked experiment 1, the release point was outside the home range because the tagged fish that homed were not tracked and monitored near the release point after homing (Figs. 3a and 4a). Although black rockfish can home using landmarks from outside the home range if they use the area map developed while searching for a suitable habitat when young (Matthews, 1990), our experimental results show that black rockfish use not vision, but olfactory cues for homing from outside the home range. There would be little advantage for black rockfish in memorizing the geographical features outside the home range that they learned when young because there would be little likelihood in daily life of being displaced outside the home range by strong currents or tides. Furthermore, in this study, 14 of the 18 homing rockfish returned to their habitats between dusk and dawn. Clearly, vision is used less under low light conditions than during the day, which implies a limitation in the use of vision for homing in black rockfish. However, the fish displaced to an unfamiliar area could determine their positions relative to the home site. This fact suggests that the rockfish in the unfamiliar area could exploit a stimulus from the familiar area. Therefore, the black rockfish must use olfaction as its main navigational cue. The black rockfish moved at random along currents just after displacement (Mitamura et al., 2002). During this period the fish might search for a similar stimulus to detect the home ward detection, although the handling and tagging trauma might prevent the fish from carrying the random movements. Further studies of homing migration, including the monitoring of water currents, are needed to clarify how black rockfish find the right direction from the olfactory cues. Subsequently, the fish started to home after recognizing a previously experienced stimulus. However, it is unclear what olfactory cues the black rockfish uses for homing. We can hypothesize three kinds of olfactory cues

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that could be used in homing because black rockfish do not move over extensive areas of habitat but form schools at one location (Harada, 1962). The first possibility is an olfactory-cue characteristic of the habitat. The black rockfish might home using a characteristic habitat olfaction similar to that of the salmonids (Doving et al., 1985; Kitahashi et al., 2000; Tanaka et al., 2000). The second possibility is an olfactory cue from substances, for example urine, used as individual markers. The third possibility is an olfactory cue provided by conspecifics inhabiting the same home range (Sweatman, 1988; Polkinghorne et al., 2001). It is evident that black rockfish in rocky areas primarily use olfaction to home, as do salmon in open waters, although other site-specific fish often use vision to orient themselves (Doving and Stabell, 2003; Dodson, 1988; Reese, 1989). The black rockfish is nocturnal and does not live in very clear waters. Therefore, it may have developed olfactory cues rather than visual cues for orientation because it is easier to use olfaction than vision during the night time. However, the question bWhat is the olfactory cue for home?Q remains to be answered. Some recent reports showed that the nose of another homing fish, the rainbow trout Oncorhynchus mykiss, may also detect the Earth’s magnetic field (Walker et al., 1997; Diebel et al., 2000). The possibility that the black rockfish uses magnetic fields as well as olfaction in their homing mechanism might not be discounted. 4.2. Advantages of homing and habitat fidelity The black rockfish congregates at specific places and territories, especially males during the reproductive season (Harada, 1962; Shinomiya and Ezaki, 1991). Moreover, the rockfish copulates in its habitat (Shinomiya and Ezaki, 1991). These facts suggest that homing ability and habitat fidelity may optimize their chances of acquiring future breeding partners and facilitates higher reproductive success than could be achieved by drifting among likely habitats. In our olfactory-cue experiment, mature black rockfish without ablation returned home through the habitat of the tanker berth, which is potentially a better habitat than their original habitat. These results indicate that once black rockfish have succeeded in reproducing in a habitat,

they may prefer the known environmental conditions to those that are unknown. In contrast, half the mature olfaction-ablated rockfish did not find the homeward direction and stayed at the potentially better habitat rather than their original home. This indicates that they selected the new area where a higher reproductive success could be achieved than other areas. In each visual-block experiment, the smallest fish did not return home. Immature rockfish do not seem to have homing ability (Carlson and Haight, 1972). During the reproductive season, small male black rockfish establish smaller and more peripheral territories than those of larger males and have minimal opportunities for courtship because they are occasionally chased and butted by larger territorial males (Shinomiya and Ezaki, 1991). These facts indicate that the advantages of homing and location fidelity may be greater for experienced mature adults than for immature fish that are unlikely to achieve reproductive success in their existing habitats. There may be a reproductive advantage in young rockfish not returning home but colonizing new habitat where they have a better chance of growing to maturity.

Acknowledgements This study required the help of many people. We thank M. Ueno and R. Masuda, of the Graduate School of Agriculture, Kyoto University, for their kind advice and support of the experiment. We thank T. Maruo, of Fisheries and Environmental Oceanography, Graduate School of Agriculture, Kyoto University, for his help to fish Mebaru and for his daily encouragement. We thank Captain K. Sato, who operated the research vessel. We also thank H. Ueda of the Field Science Center for the Northern Biosphere, Hokkaido University, for kind comments about the methods used in this study. [RH]

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